Uncoupling of behavioral and metabolic 24-h rhythms in reindeer

Abstract

Reindeer in the Arctic seasonally suppress daily circadian patterns of behavior present in most animals.¹ In humans and mice, even when all daily behavioral and environmental influences are artificially suppressed, robust endogenous rhythms of metabolism governed by the circadian clock persist and are essential to health.^2,3 Disrupted rhythms foster metabolic disorders and weight gain.⁴ To understand circadian metabolic organization in reindeer, we performed behavioral measurements and untargeted metabolomics from blood plasma samples taken from Eurasian tundra reindeer (Rangifer tarandus tarandus) across 24 h at 2-h intervals in four seasons. Our study confirmed the absence of circadian rhythms of behavior under constant darkness in the Arctic winter and constant daylight in the Arctic summer, as reported by others.¹ We detected and measured the intensity of 893 metabolic features in all plasma samples using untargeted ultra-high-performance liquid chromatography-mass spectrometry (UPLC-MS). A core group of metabolites (66/893 metabolic features) consistently displayed 24-h rhythmicity. Most metabolites displayed a robust 24-h rhythm in winter and spring but were arrhythmic in summer and fall. Half of all measured metabolites displayed ultradian sleep-wake dependence in summer. Irrespective of the arrhythmic behavior, metabolism is rhythmic (24 h) in seasons of low food availability, potentially favoring energy efficiency. In seasons of food abundance, 24-h rhythmicity in metabolism is drastically reduced, again irrespective of behavioral rhythms, potentially fostering weight gain.

Keywords: 24-h rhythms; Arctic; NDVIQ3; UPLC-MS; blood metabolomics; caribou; circadian rhythms; metabolism; reindeer; seasonality.